Gelatinous matrix, an original convergent evolution to cope with oligotrophy in Nassellaria (Radiolaria)

Abstract

Radiolaria are heterotrophic protists abundant in the world's oceans playing important roles in oceanic biogeochemical cycles. Some species can host photosynthetic algae thus contributing to primary production. Such mixotrophic behaviour is believed to explain their ecological success in oligotrophic waters, notably Collodaria, a group of exclusively mixotrophic radiolarians embedded in a gelatinous matrix. Sampling oligotrophic California Current communities revealed an abundant, rarely observed population of Nassellaria of the genus Phlebarachnium, the only Radiolaria known to live within a gelatinous matrix besides Collodaria. Phylogenetic reconstruction of the ribosomal DNA suggests that these two distantly related lineages within Nassellaria independently developed the ability to produce a gelatinous matrix ~120 million years ago. Molecular analyses identify photosynthetic symbionts as Scrippsiella sp., a common dinoflagellate symbiont of other planktonic groups. By matching our physical samples with their genetic signature, we identified these rarely observed organisms in global metabarcoding datasets, revealing a strong biogeographic affinity to oligotrophic water masses. Our results suggest that the gelatinous matrix is an exclusive adaptation to oligotrophic waters although further research is required to evaluate the similarities between the gelatinous matrices of Collodaria and Phlebarachnium. We hypothesize that such an original convergent evolution could increase the effective volume to weight ratio favoring prey contact and capture and provide an advantageous microenvironment for symbionts, enhancing ecological success in nutrient-depleted waters. This study advances our understanding of the evolution of eukaryotic diversity and highlights the specific advantages of certain adaptations, specifically when evolution occurs independently among various lineages.